ARTICLE Received 18 Feb 2013 | Accepted 8 Aug 2013 | Published 10 Sep 2013 DOI: 10.1038/ncomms3423 Soft tissue preservation in a fossil marine lizard with a bilobed tail fin Johan Lindgren1, Hani F. Kaddumi2 & Michael J. Polcyn3 Mosasaurs are secondarily aquatic squamates that became the dominant marine reptiles in the Late Cretaceous about 98–66 million years ago. Although early members of the group possessed body shapes similar to extant monitor lizards, derived forms have traditionally been portrayed as long, sleek animals with broadened, yet ultimately tapering tails. Here we report an extraordinary mosasaur fossil from the Maastrichtian of Harrana in central Jordan, which preserves soft tissues, including high fidelity outlines of a caudal fluke and flippers. This specimen provides the first indisputable evidence that derived mosasaurs were propelled by hypocercal tail fins, a hypothesis that was previously based on comparative skeletal anatomy alone. Ecomorphological comparisons suggest that derived mosasaurs were similar to pelagic sharks in terms of swimming performance, a finding that significantly expands our under- standing of the level of aquatic adaptation achieved by these seagoing lizards. 1 Department of Geology, Lund University, 223 62 Lund, Sweden. 2 Eternal River Museum of Natural History, Amman 11123, Jordan. 3 Roy M. Huffington Department of Earth Sciences, Southern Methodist University, Dallas, Texas 75275, USA. Correspondence and requests for materials should be addressed to J.L. (email: [email protected]). NATURE COMMUNICATIONS | 4:2423 | DOI: 10.1038/ncomms3423 | www.nature.com/naturecommunications 1 & 2013 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3423 onvergent evolution has resulted in some remarkable Results morphological adaptations in organisms that are found in Geological context and age. The specimen comes from the Csimilar environments. A classic example is the streamlined Muwaqqar Chalk Marl Formation (MCMF), which is part of body shape and fluked tail developed by cetaceans and fish to the Belqa Group, and spans the Cretaceous/Paleogene boundary. allow swift movement through the water. Piscine body plans and The sediments were deposited on the southern margin of the bilobed caudal flukes have also been documented in two groups of Neo-Tethys Ocean26. The strata comprise mainly chalk and distantly related Mesozoic marine reptiles; that is, ichthyosaurs locally bituminous chalky marl with abundant limestone and and metriorhynchid crocodyliforms, thanks to rare soft tissue chert concretions, and have been interpreted as a deep-water impressions in exceptionally preserved fossils1–3. However, to pelagic deposit26. The MCMF is part of a larger Upper date, no similar soft tissue evidence has been reported in Cretaceous–Eocene carbonate and phosphate sequence that mosasaurs, despite a remarkably rich fossil record and a extends across northern Africa and into the Middle East27. collection history that spans almost 250 years4. This lack of Phosphatic deposits formed in areas of high primary productivity evidence, combined with conflicting hypotheses of the are known to preserve abundant vertebrate fossils, including phylogenetic affinities of mosasaurs within Squamata5–9, have remains of, for example, mosasaurs, plesiosaurs, sharks, bony fish, fuelled the cliche´ serpentine and lizard-like depictions of turtles and marine crocodylians27,28. With the notable exception mosasaurs that dominate both the scientific and popular of ref. 25, reports of Cretaceous vertebrates from the phosphatic literature10–13. Moreover, studies of locomotor performance in deposits of Jordan have hitherto been based on a relatively limited mosasaurs have been hampered, because they have largely relied material; however, the fossils indicate a diverse fauna similar in on incorrect descriptions and reconstructions of the derived composition to that of Morocco28–31. On the basis of sequence mosasaur body plan (that is, a long, rectilinear body and straight, stratigraphy26 and microfaunal composition32, the oldest fossils elongate tail). These errors in assumption have lead to the from the MCMF are early to mid-Maastrichtian in age, although hypothesis that mosasaurs were slow-swimming animals capable the age of the remaining Cretaceous part of the formation is of only short burst of speed during brief ambush pursuits2,11,14–16. unknown (including its precise age in the Harrana area and Although early members of the group almost certainly utilized an whether or not it reaches the Cretaceous/Paleogene boundary). undulating motion as a primary means of propulsion, the question remains how far the subsequent, better aquatically adapted forms The specimen. ERMNH HFV 197 was collected in 2008 from a came toward achieving a more energy-efficient, sustained single micritic limestone concretion by one of us (HFK). The swimming style. specimen has been cleaved along the sagittal plane and is disposed Fundamental to our understanding of mosasaur locomotion, on two main slabs (collectively registered as ERMNH HFV 197- and the degree of aquatic adaptation they achieved, is knowl- A) and a counterpart (ERMNH HFV 197-B), displaying a largely edge of the form, function and development of their tail flukes. articulated mosasaur skeleton that is complete, save for the head Historically, the predominant view was that the fin-like and distal fourth of the tail (Fig. 1). The bones are generally in a extremity, of even derived mosasaurs, was virtually straight pristine condition and retain their original three-dimensional and spatulate, ‘like that of a great eel’17. Reconstructions of 18 shape, although some skeletal elements were fractured or lost crescent-shaped flukes were few andweredismissedasbeing during the excavation of the fossil; the latter are now represented based on poorly preserved specimens11,orviewedasinconflict 10,11 by natural moulds. In addition, plant rootlets have penetrated and with existing skeletal evidence . Nonetheless, over the last partially dissolved a string of vertebrae near the end of the tail. few years a growing body of data gathered from morphometric The exposed elements of the pectoral girdle and rib cage are and comparative anatomical studies have indicated that the somewhat disturbed and the latter structure has suffered slight distal third of the mosasaur tail was structurally downturned in crushing; otherwise, the skeleton is in nearly perfect articulation, life and, in that regard, was similar to the hypocercal caudal preserving, for example, a virtually complete, hydrofoil-like flukes of derived ichthyosaurs and metriorhynchid 19–23 21–23 forelimb surrounded by skin impressions (Figs 1 and 2) and the crocodyliforms . It has even been suggested that original configuration of the fan-like structure formed by the certain advanced forms had semilunate tails resembling those neural spines in the posteriormost intermediate caudal and of pelagic sharks (although dorsoventrally mirrored), but until terminal caudal series (Figs 1 and 3a,b). nownosofttissueevidencetosupporttheseclaimshasbeen reported. Here we describe an exquisitely preserved specimen (ERMNH Taxonomy. ERMNH HFV 197 was originally described in 2009 HFV 197; Eternal River Museum of Natural History) of a small- and was designated as the holotype of Tenerasaurus (from sized mosasaurine mosasaur from the Upper Cretaceous Tenera, La., young or immature; sauros, Gr., lizard) hashimi in recognition of its small size (as preserved, B1.5 m in length) and (Maastrichtian) Konservat-Lagersta¨tte of Harrana in central 25 Jordan. The fossil has been mentioned previously in an abstract24 presumed juvenile ontogenetic stage . Within Mosasauridae, possession of fused haemal arch–spine complexes supports and its skeletal morphology has been generally examined in a 6 book chapter25. Here, however, we report the full preparation of referral to the subfamily Mosasaurinae . The skeletal anatomy of Tenerasaurus agrees in all observable respects with the generic ERMNH HFV 197, including unique details of its soft tissue 33 anatomy. In addition to being largely articulated and complete diagnosis of the genus Prognathodon and is therefore referred to from the fifth cervical vertebra to the distal fourth of the caudal that taxon here. This taxonomic reassignment is also supported segment, the fossil preserves in great fidelity a gentle ventral by the fact that Prognathodon is represented by numerous larger individuals in the MCMF25 and more broadly in the Middle East tailbend and large portions of integument, revealing, for the first 34,35 time in a mosasaur, the soft tissue outline of a tail fin. ERMNH and Africa . HFV 197 provides definitive evidence that derived mosasaurines were propelled by bilobed, asymmetrical caudal flukes, to Discovery of soft tissues. During examination of ERMNH HFV demonstrate that mosasaurs are convergent with ichthyosaurs, 197 in December 2011, the senior author (JL) discovered what metriorhynchid crocodyliforms and whales in the development of appeared to be soft tissue remains surrounding the distalmost a specialized, crescent-shaped propulsive surface for enhanced portion of the caudal vertebral column. This prompted a re- locomotor efficiency. investigation of the fossil with the aim of exposing further skin 2 NATURE COMMUNICATIONS | 4:2423 | DOI: 10.1038/ncomms3423 | www.nature.com/naturecommunications & 2013 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3423